Diptera Cecidomyiidae), a New Inquiline Gall Midge Species from Galls of Dasineura Mali on Apple in Italy

Home , Cecidomyiidae, Ptychopteromorpha

Bulletin of Insectology 58 (2): 95-99, 2005 ISSN 1721-8861 Description of Macrolabis mali sp. nov. (Diptera Cecidomyiidae), a new inquiline gall midge species from galls of Dasineura mali on apple in Italy

1 2 3 1 Gianfranco ANFORA , Nunzio ISIDORO , Antonio DE CRISTOFARO , Claudio IORIATTI 1Istituto Agrario di San Michele all’Adige (IASMA), San Michele all’Adige, Trento, Italy 2Dipartimento di Scienze Ambientali e delle Produzioni Vegetali, Università Politecnica delle Marche, Ancona, Italy 3Dipartimento di Scienze Animali, Vegetali e dell’Ambiente, Università degli Studi del Molise, Campobasso, Italy

Abstract

Macrolabis mali Anfora sp. nov. (Diptera Cecidomyiidae) is described and its taxonomically important structures are illustrated. Larvae live as inquilines in leaf galls of Dasineura mali (Kieffer) on Malus domestica Borkhausen. The new species was found in orchards of Trento Province (Italy) during summer 2003. The basic biology of the new species is reported.

Key words: Cecidomyiidae, Diptera, Macrolabis mali, Dasineura mali, gall midges, Malus domestica, apple, Rosaceae, inquiline, insect taxonomy.

Introduction Below we provide a description of the species, called Macrolabis mali sp. nov., collected from apple leaf galls The Apple Leaf Curling Midge, Dasineura mali in Trento Province. Studies were carried out by the en- (Kieffer) (Diptera Cecidomyiidae), damages cultivated titled authors, while this description by G. Anfora. apple trees in Europe, Asia, North America, and New Zealand; the larvae feed on fluids of tissue of young developing leaves and cause the edges to roll tightly in- Materials and methods wards along the central nervure, to swell (reddish galls), and to drop prematurely. D. mali control requires pesti- Leaf galls infested with midge larvae were collected cide applications, especially in nurseries and young from organic Malus domestica Borkhausen (Rosaceae, plantations (Antonin and Baggiolini, 1972). In 2003 and cv. Golden, Stark, Fuji) orchards in Trento Province 2004, during studies on D. mali, another midge species (Northern Italy) in spring and summer 2003 and 2004. emerged from apple leaf galls collected in Trento Prov- Some leaves were dissected, the mature larvae were di- ince (Italy). This new species is placed in the Palaearctic vided by species, and preserved in 70% ethanol. To rear genus Macrolabis Kieffer ,1892, comprising 52 species; adult midges, some galls were placed in cubic plastic Macrolabis species are both gall-making and inquilines, cages (length 45 cm) with a 3-cm layer of horticultural and usually monophagous on host plants belonging to 21 soil, where the larvae of both species could pupate. families (Skuhravá, 1986; Fedotova, 2000). The presence Cages were housed in a climatic chamber (26 ± 2 °C, 60 of a Macrolabis species in apple orchards has been pre- ± 5% R.H., L16:D8 photoperiod). The emerged adults viously signalled only in South Tyrol to SW Germany, were preserved in 70% ethanol. The insect morphology and it was considered a gall-maker (Carl, 1980). The was studied using bright field and phase contrast mi- new species is not included in the last review of the genus croscopy. Permanent microscope slides were obtained (Fedotova, 2000) and in the checklists of the gall midge for the type series; the specimens were prepared ac- fauna in Italy (Skuhravá and Skuhravý, 1994; Dahl et al., cording to the technique proposed by Gisin (1960) for 1995), Switzerland (Skuhravá and Skuhravý, 1997), Collembola, emptying the larval body after the clearing Austria (Skuhravá and Skuhravý, 1995), and Southern treatment. Some adults were also mounted on pinned Tyrol (Skuhravá et al., 2001). It is also not mentioned paper labels using the Faurè liquid. among the midges infesting plants of the family Rosa- ceae (Fedotova 2002a; 2002b). Given the shape of the galls, which differs from that of the galls of other gall- Results making Macrolabis species (Fedotova, 2000), the pre- liminary studies on its biology (Anfora et al., 2005) and Type material other still unpublished data, we suggest that the new spe- The holotype and part of the paratypes, mounted in cies is not a gall-maker, but an inquiline, normally Canada balsam on permanent microscope slides, are de- dwelling in D. mali galls. In England, another Macrola- posited at the Tridentino Natural Sciences Museum bis species was reported as an inquiline in galls of Dasi- (TNSM) (Trento, Italy). The other paratypes, preserved neura pyri (Bouchè) (Barnes, 1948), but it has not been in 70% ethanol and mounted, and the slides are depos- found in north alpine area (Carl, 1982) and in pear or- ited at the Research Center of Agricultural Institute of S. chards of northern Italy (personal observations, 2004). Michele all’Adige (Trento, Italy). Figures 1-7. Macrolabis mali sp. nov. male. (1) Adult. (2) Flagellar segments. (3) Palpus. (4) Tarsal claw and empodium. (5) Wing. (6) Genitalia in dorsal view (cerci, hypoproct, and mediobasal lobes of gonocoxites). (7) Genitalia in dorsal view (gonocoxite and gonostylus). (In colour at www.bulletinofinsectology.org).

96 Figures 8-12. Macrolabis mali sp. nov. female. (8) Adult. (9) Flagellar segments. (10) Palpus. (11) Tarsal claw and empodium. (12) Apex of ovipositor in lateral view. Figure 13. Anterior part of Macrolabis mali sp. nov. larva. (In colour at www.bulletinofinsectology.org).

Holotype male, S. Michele all’Adige (46°11’N, than others, 0.4 times as long as 10th. Palpal segment 11°07’E), 15 km N of Trento (NE Italy), ex leaf gall on length ratio 5:9:11:15; palpiger distinct, 4th segment M. domestica collected 27.VI.2003, emerged 13.VII.2003 slightly dilated in distal half and rounded apically. Tar- (leg. G. Anfora), TNSM n° 1. Paratypes 10 females, 9 sal claw arcuately rounded basally, with long and wide, males, same locality and date as holotype, TNSM n° 2- nearly backwards-directed, tooth at base; empodium 20. Other material collected from orchards of the whole slightly longer than claw. Wing the widest in distal half, Trento Province during summer 2003 and 2004. 2.5 times as long as wide; vein R5 slightly curved, join- ing costa before the wing apex, Cu forked; veins R5 and Description Cu running into wing margin at nearly equal distances from wing apex. Gonocoxite large and swollen, asym- Male (figures 1-7) metrical, with widely rounded outer side and nearly Body length 1.0-1.5 mm (1.26 ± 0.17 mm; n=10). straight inner side, about 1.3 times as long as wide. Colour thorax and abdomen yellowish pale orange. An- Gonostylus slender, half as long as gonocoxite, strongly tennae 2 + 11-segmented, flagellar segments separated, swollen and rounded at base, dorsal side nearly straight, without stems, 2nd segment 1.1 times as long as 1st, 5th ventral rounded, nearly parallel-sided before apex, 1.15 times as long as wide, 9th 1.2 times as long as 10th; pointed apically, 3.3 times as long as wide. Cerci with 11th appendage-like, conical and separated, narrower long oval lobes divided by wide triangular rounded inci-

97 sion and with a little lateral prominence at half. Hypo- proct 0.7 times as long as cerci and 0.3 times as wide as cerci, slightly dilated toward base with wide oval inci- sion apically between long and fine lobes. Mediobasal lobe of gonocoxites apically pointed and indented, gradually dilated to base. Genitalia infuscate, with sur- face looking rough because of spotted relief.

Female (figures 8-12) Body length 1.1-1.5 mm without ovipositor (1.32 ± 0.13 mm; n=10). Colour as in male. Antennae 2 + 12- segmented; 1st flagellar segment slightly narrowing at base and as long as 2nd; 5th segment 1.2 times as long as wide; 12th ovoid, narrower than others, 1.1 times as long as 11th. Palpal segment length ratio 3:4:5:7; palpiger distinct, 4th segment slightly dilated laterally and rounded apically. Tarsal claw nearly semicircular with long and wide, nearly backwards-directed, tooth at base; Figure 14. Leaf galls of Dasineura mali (Kieffer) on empodium slightly longer than claw. Ovipositor with apple. fused cerci (= apical plate) which, in lateral view, is (In colour at www.bulletinofinsectology.org). slightly narrowing toward apex and nearly pointed apically; the latter looking infuscate because of more densely arranged microtrichiae. Apical plate 2.8 times becomes larger than that of the host. The larvae of the as long as wide. gall inducer may thus die because of the large number of inquilines as it is known in M. luceti larvae of which Larva (figure 13) may cause the withering of larvae of the gall causer, W. Colour whitish-yellow. Length 2.3-2.5 mm (2.39 ± rosarum on Rosa spp. (Robbins, 2000). 0.12 mm; n=20). Head with antennae 0.3 times as long as head capsule, posterolateral apodemes about as long Etimology as head capsule. Sternal spatula orange-brown with long The specific name of this taxon is derived from the stem and anterior part divided by long and pointed generic name of the host plant. lobes; a lateral papilla each side of spatula. Terminal segment with four pairs of papillae setose. Acknowledgements Differential diagnosis Macrolabis mali sp. nov. is similar in biology and This research has been supported by the Autonomous morphological characters to Macrolabis luceti Kieffer Province of Trento (Research Project SEDAMA). and Macrolabis alatauensis Fedotova, which both live We thank Bruno Maiolini (Tridentino Natural Sci- as inquilines in galls of Wachtliella rosarum (Hardy) ences Museum, Trento) for his kindly help in the insect (Diptera Cecidomyiidae) on various species of Rosa preparation, Edith Ladurner (La.Me.Ba. s.a.s.) for the (Rosaceae). The three species are related because of the language review, Monica Sofia, Ivan Enrici and Fede- arrangement of the whole wing and the hypoproct rico Pedrazzoli (IASMA) for technical assistance. We length. The relation between M. mali sp. nov. and M. also thank the anonymous reviewers for careful com- luceti is also due to the shape of the hypoproct and the ments. length of the apical plate of the ovipositor, while that between M. mali sp. nov. and M. alatauensis is due to the shape of the gonostylus and the structure of the fe- References male antenna. M. mali sp. nov. considerably differs from the latter species in the cerci (lobes long and ANFORA G., IORIATTI C., MOSER S., GERMINARA G. S., DE CRISTOFARO A., 2005.- Electrophysiological responses of widely divided), in the shape of the gonocoxites and in two different species of apple gall midges (Diptera Cecido- the structure of the male antenna. myiidae) to host plant volatiles.- IOBC/wprs Bulletin, 28: in press. Biology ANTONIN P., BAGGIOLINI M, 1972.- La cécidomyie des feuilles Larvae of Macrolabis mali sp. nov. develop as in- du pommier (Dasineura mali Kieffer).- Revue Suisse de Vi- quilines in leaf galls of D. mali together with the larvae ticulture Arboriculture Horticulture, 4 (2): 51-53. of this gall-making species. The galls are reddish leaves, BARNES H. F., 1948.- Gall midges of economic importance, curled toward the midrib and swollen (figure 14). Each Vol. 3. Gall midges of fruits.- Lockwood & Son Ltd., Lon- gall usually contain 20-50 larvae of D. mali and 20-40 don, UK. CARL K. P., 1980.- Beobachtungen über die Apfelgallmücke, larvae of M. mali sp. nov.. Pupation takes place in the Dasineura mali Kieffer und eine neue Art aus Apfel- soil. In the laboratory, the pupal stage lasts 10-15 days blattgallen, Macrolabis sp. (Dipt.: Cecidomyiidae).- Anzeiger at 25 °C. Five-six generations develop per year, and, at für Schädlingskunde Pflanzenschutz Umweltschutz, 53 (7): the end of the season, the M. mali sp. nov. population 99-102.

98 CARL K. P., 1982.- Biologie, natürliche Feinde und ROBBINS J., 2000.- Some observations on Macrolabis luceti Bekämpfung der Birnenblattgallmücke, Dasineura pyri.- Kieffer: (Diptera, Cecidomyiidae).- Cecidology, 15 (1): 76. Erwerbobstbau, 24 (7): 166-169. SKUHRAVÁ M., 1986.- Family Cecidomyiidae, pp. 72-297. In: DAHL C., KRIVOSHEINA N. P., KRZEMINSKA E., LUCCHI A., Catalogue of Palaearctic Diptera, Vol. 4, Sciaridae- NICOLAI P., SALAMANNA G., SANTINI L., SKUHRAVÁ M., Anisopodidae.- Akademiai Kiado, Budapest, HU. ZWICK P., 1995.- Diptera Blephariceromorpha, Bibionomor- SKUHRAVÁ M., SKUHRAVÝ V., 1994.- Gall midges (Diptera: pha, Psychodomorpha, Ptychopteromorpha, pp. 23-32. In: Cecidomyiidae) of Italy.- Entomologica, 28: 45-76. Checklist delle specie della fauna italiana 64 (MINELLI A., SKUHRAVÁ M., SKUHRAVÝ V., 1995.- Die Gallmücken von RUFFO S., LA POSTA S., Eds).- Calderini, Bologna, Italy. Österreich II.- Sitzungsberichte der Österreichischen FEDOTOVA Z. A., 2000.- A review of gall midges of the genus Akademie der Wissenschaften, 201: 3-34. Macrolabis Kieffer (Diptera, Cecidomyiidae) with descrip- SKUHRAVÁ M., SKUHRAVÝ V., 1997.- Gall midges (Diptera: tion of new species from Kazakhstan.- Entomological Re- Cecidomyiidae) of Switzerland.- Mitteilungen Schweizeris- view, 80 (6): 620-634. chen Entomologischen Gesellschaft, 70: 133-176. FEDOTOVA Z. A., 2002a.- Gall midges (Diptera, Cecidomyii- SKUHRAVÁ M., SKUHRAVÝ V., HELLRIGL K., 2001.- Die dae) developing on Rosaceae in Palaearctic and a summary Gallmückenfauna (Cecidomyiidae, Diptera) Südtirols ein of the Kazakhstan fauna, Report 1.- Entomological Review, Beitrag zür Gallmückenfauna Italiens.- Gredleriana, 1: 83- 81 (1): 60-70. 132. FEDOTOVA Z. A., 2002b.- Gall midges (Diptera, Cecidomyii- dae) developing on Rosaceae in Palaearctic and a summary of the Kazakhstan fauna, Report 2.- Entomological Review, Corresponding author 81 (1): 201-211. Claudio IORIATTI ([email protected]), Unità Operativa GISIN H., 1960.- Collembolenfauna Europas.- Musee Histoire Difesa delle Colture e Selezione Sanitaria, Istituto Agrario di Naturelle, Geneve, CH. San Michele all’Adige, Via E. Mach 1, I-38010 S. Michele KIEFFER J. J., 1892.- Beobachtungen über Gallmücken mit a/A (TN), Italy. Beschreibung einiger neuen Arten.- Wiener Entomologische Zeitung, 11: 212-224. Received May 2, 2005. Accepted September 5, 2005.